Inherited proliferation states organize plant transcriptomes

Expression variation in natural plant populations is usually read gene by gene, as a response to the environment. Whether a leading axis of that variation is more strongly associated with ancestry than with home-site environment, and whether it is heritable, remain unresolved. We integrated transcriptomes, genotypes, environmental records and phenotypes from 665 Arabidopsis thaliana accessions grown under one condition. Genomic ancestry uniquely explained 5.0% of the dominant expression axis, compared with 2.6% for home-site environment, and exceeded environment under all four allocations of geography and the circadian covariate (1.9- to 6.2-fold). This axis was associated with a heritable cell-cycle- and ribosome-enriched module (prolifME; h^2 = 0.19), linked to four loci with widespread trans-expression associations and associated with smaller plants in two independent experiments and with slower growth under controlled conditions. The advantage is concentrated on the leading expression axes and narrows across the full transcriptome. The gene weights defining the Arabidopsis axis were correlated with independently derived profiles in rice and maize, with the correspondence carried mainly by photosynthesis-associated genes. Ancestry therefore predicts the leading expression axes, and the heritable proliferation module that carries the first axis tracks growth phenotypes independently of ancestry.